Loading of nitrate into the xylem: apoplastic nitrate controls the voltage dependence of X‐QUAC, the main anion conductance in xylem‐parenchyma cells of barley roots

Köhler, Barbara; Wegner, Lars H.; Осипов, В. И.; Raschke, Klaus

doi:10.1046/j.1365-313x.2002.01269.x

Cited by 61 publications

(51 citation statements)

References 43 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Two of these, an inwardly rectifying anion channel (X-IRAC) and a quickly activating anion conductance (X-QUAC), are nitrate permeable and may be involved in the xylem loading of nitrate. Further studies have shown that X-IRAC and X-QUAC are differentially regulated by water stress (Gilliham and Tester, 2005) and that the voltage dependence of X-QUAC is regulated by apoplastic nitrate, suggesting that xylem loading of nitrate is subject to delicate regulation (Kö hler et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Mutation of the Arabidopsis NRT1.5 Nitrate Transporter Causes Defective Root-to-Shoot Nitrate Transport

et al. 2008

View full text Add to dashboard Cite

Little is known about the molecular and regulatory mechanisms of long-distance nitrate transport in higher plants. NRT1.5 is one of the 53 Arabidopsis thaliana nitrate transporter NRT1 (Peptide Transporter PTR) genes, of which two members, NRT1.1 (CHL1 for Chlorate resistant 1) and NRT1.2, have been shown to be involved in nitrate uptake. Functional analysis of cRNA-injected Xenopus laevis oocytes showed that NRT1.5 is a low-affinity, pH-dependent bidirectional nitrate transporter. Subcellular localization in plant protoplasts and in planta promoter-b-glucuronidase analysis, as well as in situ hybridization, showed that NRT1.5 is located in the plasma membrane and is expressed in root pericycle cells close to the xylem. Knockdown or knockout mutations of NRT1.5 reduced the amount of nitrate transported from the root to the shoot, suggesting that NRT1.5 participates in root xylem loading of nitrate. However, root-to-shoot nitrate transport was not completely eliminated in the NRT1.5 knockout mutant, and reduction of NRT1.5 in the nrt1.1 background did not affect rootto-shoot nitrate transport. These data suggest that, in addition to that involving NRT1.5, another mechanism is responsible for xylem loading of nitrate. Further analyses of the nrt1.5 mutants revealed a regulatory loop between nitrate and potassium at the xylem transport step. INTRODUCTIONNitrate and ammonium ions are the two major nitrogen sources for higher plants. Due to its toxicity, ammonium is preferentially assimilated in the root and then transported in an organic form to the aerial parts. By contrast, nitrate can be assimilated into ammonium and then amino acids in the root or shoot. Partitioning of nitrate assimilation between the root and shoot depends on the plant species, external nitrate concentration, temperature, and light intensity (reviewed in Smirnoff and Stewart, 1985). If there is sufficient light, nitrate assimilation in the leaf has a lower energy cost than in the root. However, some disadvantages of leaf nitrate assimilation include (1) if light is limited, nitrate assimilation and carbon dioxide fixation will compete directly for the reductants and ATP generated by photosynthetic electron transport (Canvin and Atkins, 1974), and (2) hydroxyl ions generated in the leaf need to be neutralized by the synthesis of organic acids (in the root, the pH balance may possibly be maintained by reducing proton excretion or increasing bicarbonate excretion). Due to these factors, the partition of nitrate assimilation between the root and shoot shows both seasonal and diurnal fluctuations, allowing the plant to sustain maximal growth. In turn, the partition of nitrate assimilation depends on the partition of nitrate between the root and shoot.To transport nitrate to the aerial parts of the plant, nitrate has to be loaded into the xylem vessels of the root vascular stele. In Arabidopsis thaliana roots, four layers of cells are found surrounding the xylem, these being the epidermis, cortex, endodermis, and pericycle (in the order external to ...

show abstract

Section: Introductionmentioning

confidence: 99%

Mutation of the Arabidopsis NRT1.5 Nitrate Transporter Causes Defective Root-to-Shoot Nitrate Transport

et al. 2008

View full text Add to dashboard Cite

show abstract

“…These cells determine the anion composition of the sap flow between root and shoot (Köhler and Raschke, 2000;Köhler et al, 2002;Lin et al, 2008). Here, we used Xenopus laevis oocytes to study the anion selectivity of SLAH2 and compared it to that of SLAC1.…”

Section: Introductionmentioning

confidence: 99%

A Single-Pore Residue Renders the Arabidopsis Root Anion Channel SLAH2 Highly Nitrate Selective

et al. 2014

View full text Add to dashboard Cite

In contrast to animal cells, plants use nitrate as a major source of nitrogen. Following the uptake of nitrate, this major macronutrient is fed into the vasculature for long-distance transport. The Arabidopsis thaliana shoot expresses the anion channel SLOW ANION CHANNEL1 (SLAC1) and its homolog SLAC1 HOMOLOGOUS3 (SLAH3), which prefer nitrate as substrate but cannot exclude chloride ions. By contrast, we identified SLAH2 as a nitrate-specific channel that is impermeable for chloride. To understand the molecular basis for nitrate selection in the SLAH2 channel, SLAC1 and SLAH2 were modeled to the structure of HiTehA, a distantly related bacterial member. Structure-guided site-directed mutations converted SLAC1 into a SLAH2-like nitrate-specific anion channel and vice versa. Our findings indicate that two pore-occluding phenylalanines constrict the pore. The selectivity filter of SLAC/SLAH anion channels is determined by the polarity of pore-lining residues located on alpha helix 3. Changing the polar character of a single amino acid side chain (Ser-228) to a nonpolar residue turned the nitrate-selective SLAH2 into a chloride/nitrate-permeable anion channel. Thus, the molecular basis of the anion specificity of SLAC/SLAH anion channels seems to be determined by the presence and constellation of polar side chains that act in concert with the two pore-occluding phenylalanines.

show abstract

“…The ALAACs of wheat and maize roots (see above) resemble S-type channels in that they display slow activation kinetics (Pineros and Kochian, 2001;Zhang et al, 2001) and exhibit inwardly rectifying current voltage relationships. Other reports of anion channel activity in roots are limited to an outwardly rectifying anion-selective channel in wheat and maize, which allows anion influx from the soil solution (Skerrett and Tyerman, 1994;Pineros and Kochian, 2001) and three different anion conductances in the xylem parenchyma cells of barley (Hordeum vulgare) roots, which are thought to mediate anion efflux to the xylem vessels during salt delivery to the shoot (Kohler and Raschke, 2000;Kohler et al, 2002). In particular, there has been no systematic study of anion channels in roots with respect to root soil interaction and nutrient acquisition.…”

mentioning

confidence: 99%

“…Anion efflux channels have also been characterized in the xylem parenchyma cells of barley roots (Kohler and Raschke, 2000;Kohler et al, 2002) where they are proposed to mediate anion transport into the xylem vessels. In these studies, three anion efflux channel types were identified.…”

mentioning

confidence: 99%

Characterization of Anion Channels in the Plasma Membrane of Arabidopsis Epidermal Root Cells and the Identification of a Citrate-Permeable Channel Induced by Phosphate Starvation

et al. 2004

View full text Add to dashboard Cite

Organic-acid secretion from higher plant roots into the rhizosphere plays an important role in nutrient acquisition and metal detoxification. In this study we report the electrophysiological characterization of anion channels in Arabidopsis (Arabidopsis thaliana) root epidermal cells and show that anion channels represent a pathway for citrate efflux to the soil solution. Plants were grown in nutrient-replete conditions and the patch clamp technique was applied to protoplasts isolated from the root epidermal cells of the elongation zone and young root hairs. Using SO 4 22 as the dominant anion in the pipette, voltagedependent whole-cell inward currents were activated at membrane potentials positive of 2180 mV exhibiting a maximum peak inward current (I peak ) at approximately 2130 mV. These currents reversed at potentials close to the equilibrium potential for SO 4 22 , indicating that the inward currents represented SO 4 22 efflux. Replacing intracellular SO 4 22 with Cl 2 or NO 3 2 resulted in inward currents exhibiting similar properties to the SO 4 22 efflux currents, suggesting that these channels were also permeable to a range of inorganic anions; however when intracellular SO 4 22 was replaced with citrate or malate, no inward currents were ever observed. Outside-out patches were used to characterize a 12.4-picoSiemens channel responsible for these whole-cell currents. Citrate efflux from Arabidopsis roots is induced by phosphate starvation. Thus, we investigated anion channel activity from root epidermal protoplasts isolated from Arabidopsis plants deprived of phosphate for up to 7 d after being grown for 10 d on phosphate-replete media (1.25 mM). In contrast to phosphate-replete plants, protoplasts from phosphatestarved roots exhibited depolarization-activated voltage-dependent citrate and malate efflux currents. Furthermore, phosphate starvation did not regulate inorganic anion efflux, suggesting that citrate efflux is probably mediated by novel anion channel activity, which could have a role in phosphate acquisition.

show abstract

Loading of nitrate into the xylem: apoplastic nitrate controls the voltage dependence of X‐QUAC, the main anion conductance in xylem‐parenchyma cells of barley roots

Cited by 61 publications

References 43 publications

Mutation of the Arabidopsis NRT1.5 Nitrate Transporter Causes Defective Root-to-Shoot Nitrate Transport

Mutation of the Arabidopsis NRT1.5 Nitrate Transporter Causes Defective Root-to-Shoot Nitrate Transport

A Single-Pore Residue Renders the Arabidopsis Root Anion Channel SLAH2 Highly Nitrate Selective

Characterization of Anion Channels in the Plasma Membrane of Arabidopsis Epidermal Root Cells and the Identification of a Citrate-Permeable Channel Induced by Phosphate Starvation

Contact Info

Product

Resources

About